The importance of considering the evolutionary history of polyploids when assessing climatic niche evolution

Abstract

Aim Although whole‐genome duplication (WGD) is an important speciation force, we still lack a consensus on the role of niche differentiation in polyploid evolution. In addition, the role of genome doubling per se vs. later divergence on polyploid niche evolution remains obscure. One reason for this might be that the intraspecific genetic structure of polyploid complexes and interploidy gene flow is often neglected in ecological studies. Here, we aim to investigate to which extent these evolutionary processes impact our inference on niche differentiation of autopolyploids. Location Europe. Taxon Arabidopsis arenosa (Brassicaceae). Methods Leveraging a total of 352 cytotyped populations of diploid‐autotetraploid A. arenosa, we examined differences among climatic niches of diploid and tetraploid lineages both globally, and independently for each tetraploid lineage with respect to the niche of its evolutionary closest relative. Then, we tested whether there was an effect of additional interploidy introgression from other sympatric but ancestrally divergent diploid lineages of A. arenosa on climatic niches of tetraploids. Results Ecological niche shift of tetraploids is only detected when the assignment of populations to intraspecific genetic lineages is considered. We found different patterns of climatic niche evolution (i.e. niche conservatism, contraction or expansion) in each tetraploid lineage when compared to its evolutionary closest relatives. We observed an effect of interploidy gene flow in patterns of climatic niche evolution of the tetraploid ruderal lineage of A. arenosa. Main conclusions The niche shift of tetraploids in A. arenosa is not driven by WGD per se but rather reflects dynamic post‐WGD evolution in the species, involving tetraploid migration out of their ancestral area and interploidy introgression with other diploid lineages. Our study supports that evolutionary processes following WGD—which usually remain undetected by studies neglecting evolutionary history of polyploids—may play a key role in the adaptation of polyploids to challenging environments.

C4 photosynthesis provided an immediate demographic advantage to populations of the grass Alloteropsis semialata

“…We excluded polyploids, such as C 4 samples from clade IIIb (which together with IIIa form clade III), given that polyploidy has been shown to affect population success in different ways (e.g. Monnahan et al ., 2019; Padilla‐García et al ., 2023) and might confound our results. Briefly, these samples were collected during field trips between 2012 and 2019.…”

Polyploidy‐induced floral changes lead to unexpected pollinator behavior in Arabidopsis arenosa

“…A common garden for the purpose of the visitor experiment was established in Průhonice, Czech Republic (49°59'41.042''N, 14°33'55.27''E). This common garden has a similar climate to the original location of the A. arenosa populations (central Europe), and tetraploid A. arenosa grows naturally within a few kilometers of this common garden (Padilla‐García et al 2023). Therefore, we did not expect major changes in the insect visitor community between the common garden and the original locations of the A. arenosa populations, even though we were unable to exclude it.…”

Special issue.: The role of whole genome duplication in evolutionary ecology

“…To decouple the effects of polyploidy from the effect of genetic distance among independent origins in natural systems, common garden or in situ experiments that make within-lineage contrasts between diploids and their neopolyploid progeny are necessary. For observations in natural populations, we might find that controlling for genetic structure and multiple polyploid origins will allow us to detect overarching patterns, for example, as Padilla-García et al (2023) found in a study of niche divergence in Arabidopsis arenosa. There are also other factors that could obscure patterns such as the effects of evolution after WGD, divergent local adaptation across sites, or unpredictable genetic changes that arise across polyploid origins.…”

“…Second, there is a growing need to place studies of the evolutionary ecology of polyploids into a phylogenetic and population genetic context. We have known for a long time that polyploid lineages arise recurrently within species (Soltis and Soltis 1999) yet despite this recognition, few studies control for the genetic history of polyploid lineages (Padilla‐García et al 2023). This is necessary because independent polyploid origins may have different genetic backgrounds, traits, and will follow independent evolutionary trajectories.…”